Floral Dimorphism in Psychotria boninensis Nakai (Rubiaceae) Endemic to the Bonin (Ogasawara) Islands

2007·0.45 MB·English

by  Yoshimi Kondo

植物研究雑誌
J.Jpn.Bot.
Originals
82:251–258(2007)
Floral Dimorphism in Psychotria boninensis Nakai (Rubiaceae)
Endemic to the Bonin (Ogasawara) Islands
Yoshimi KONDOa, Masato NISHIDEb, Kenta WATANABEb and Takashi SUGAWARAb
aDepartmentofBiology,FacultyofScience,TokyoMetropolitanUniversity,
1–1,Minami-ohsawa,Hachioji,Tokyo,192-0397JAPAN;
bMakinoHerbarium,GraduateSchoolofScience,TokyoMetropolitanUniversity,
1–1,Minami-ohsawa,Hachioji,Tokyo,192-0397JAPAN
E-mail:[email protected]
(RecievedonMarch27,2007)
Floralandreproductivecharacterswereexaminedtodeterminemodeofdimorphism
in the flowers of Psychotria boninensis Nakai, a species endemic to the Bonin
(Ogasawara) Islands, Japan. The flowers reciprocally differed in stigma and anther
height, and were composed of long- and short-styled morphs. Pollen grains from the
short-styled morph were larger than those from the long-styled morph in size, but no
majordifferencewasfoundbetweenthetwomorphsinexinesculpture.Theshort-styled
flowersproducedlesspollengrainthanthelong-styledflowers,asinsomeothertypically
distylousspecies.Thepollengrainsproducedbythetwomorphswerepositivelystained
with Cotton Blue solution, and ovaries of the two morphs produced fruits and seeds in
field. These results suggest that the flowers of P. boninensis are morphologically
distylous,asinmostofthetypicallydistylousspecies,andthatthelong-andshort-styled
flowers are functionally bisexual. This is the first record of distyly among the plants
endemic to the Bonin Islands.
Key words: Bonin (Ogasawara) Islands, distyly, Psychotria boninensis, reciprocal
herkogamy, Rubiaceae.
Psychotria L. is a large genus comprising self and intramorph matings (Ganders 1979,
more than 1500 species and is widespread Barrett1992),althoughitisknowninseveral
from tropical to subtropical regions through- distylous species that their flowers show
out the world (Hamilton 1989, Nepokroeff self-compatibility as well as compatibility
et al. 1999). Most of the Psychotria species among the intramorphs (Riveros et al. 1995,
are shrubs or small trees, and generally grow Barrett et al. 2000). In Mesoamerican
on the forest floor. Their whitish, small Psychotria, it isnoted that of the 66 taxa 44
flowers are usually campanulate or tubiform are morphologically distylous and the others
in shape and radially symmetrical. For the are monomorphic in floral morphology
genus, the most interesting feature of the (Hamilton 1989). Meanwhile, in Hawaiian
flowers is a distyly (heterostyly) that is a ge- Psychotria, ithas been reported that all of
netically determined reciprocal herkogamy the species (11 spp.) are morphologically
ofstigmaandantherheight.Indistylousspe- distylous (Sohmer 1977, Wagner et al.
cies the flowers are composed of long- and 1990). For Japanese Psychotria species,
short-styled morphs and usually have an ad- however, available information on sexual
ditional incompatibility system that prevents dimorphism is absent.
—251—
252 植物研究雑誌 第82巻 第5号 平成19年10月
Psychotria boninensis Nakai, which is a To observe morphological differentiation,
species endemic to the Bonin (Ogasawara) several flowers after anthesis and flower
Islands, has been regarded as monomorphic buds before anthesis were randomly
in floral morphology (Ono and Kobayashi collected from the plants growing in the
1985, Yamazaki 1989, 1993, Toyoda 2003). study sites and preserved in 70(cid:1) ethanol.
However, in our preliminary study the spe- We measured five floral characters for each
cies appeared to be morphologically dimor- plant (see Fig. 1A): corolla length, corolla
phic with a distylous nature, as in other tube length, stigma height, stamen height,
species of the genus. We wonder whether P. anther length and pollen size. For measure-
boninensis is truly distylous in floral mor- ment of pollen size, anthers within a flower
phology or not. Meanwhile, in the oceanic bud before anthesis were crushed in Cotton
islands such as the Hawaiian Islands and the Blue in lactophenole. Subsequently, the
Bonin Islands, it is pointed out that dioecism polar diameter of 50 randomly selected
has frequently occurred in various taxa pollen grains was measured using a light
(Carlquist 1974, Baker and Cox 1984, microscope. The number of pollen grains per
Kawakubo 1990, Kato and Nagamasu 1995, flower was also counted in two flowers for
Sakai et al. 1995, Sugawara et al. 2004). each plant. In this case, one of the five
Actually, in the Hawaiian Islands all of the anthers within a flower bud before anthesis
Psychotria species just mentioned above are was crushed on a lattice glass slide
functionally unisexual (dioeious) despite (Matsunami Glass Ind., Ltd.) with Cotton
their distylous nature in floral morphology Blue solution under micro-binocular. In
(Wagner et al. 1990, Sakai et al. 1995). In addition, pollen stainability (fertility) of
the Bonin Islands, however, it is unclear more than 200 grains per flower was exam-
whether P. boninensis is functionally unisex- ined using aniline blue in lactophenole. For
ual or not. evaluating pollen stainability two to three
In this study, we investigated floral char- flowers per plant were examined. Ovary was
acters to determine the dimorphism in flow- sectioned transversely to ascertain ovules.
ers of Psychotria boninensis endemic to the For scanning electron microscope (SEM)
Bonin Islands and further to make clear the observation, flowers and their parts (anthers
reproductive nature of the species. and stigmas) were dehydrated in an ethanol:
t-butanol series. Dehydrated materials were
Materials and Method freezing-dried using a freeze-drying device
Psychotria boninensis Nakai is a terres- (JFD-300, JEOL), mounted onto SEM stubs
trial or climbing subshrub and occurs on the on double-sided carbon tape, coated with
floororatthemarginoftheevergreenbroad- gold using an ion sputter (JFC-1100E,
leaved forests in the Bonin (Ogasawara) JEOL) and observed using a scanning elec-
Islands, Japan. The plants concerned usually tron microscope (JSM-5600LV, JEOL).
open flowers from May to June. Their flow-
ers are relatively small, less than 5mm long, Observations
and somewhat campanulate in shape. Each Dimorphism in floral morphology
flower lasts for a single day. Fruits mature Flowers of Psychotria boninensis were
in September to October. In this study we radially symmetrical with a corolla. Corolla
examined 41 individual plants in total, tubes were short, about 2 mm long, and their
collected from Mt. Shigure-yama (alt. ca. upper portion had many oblique-facing hairs
200 m) and its surrounding area on on their inner surface (Figs. 1, 3).
Chichijima Island, the Bonin Islands. Observations of Psychotria boninensis in
October2007 JournalofJapaneseBotanyVol.82No.5 253
Fig.1. Drawingsoflong-andshort-styledmorphsofPsychotriaboninensis.A.Short-styledflower.
a. Corolla length. b. Corolla-tube length. c. Stigma height. d. Anther height. e. Anther length.
A’.Longitudinalsectionofyoungfruitintheshort-styledflower,showingtwodevelopedseeds.
B.Long-styledflower.an.Anther.co.Corollalobe.ov.Ovary.st.Stigma.sty.Style.tr.Oblique-
facinglonghairs.B’.Longitudinalsectionofyoungfruitinthelong-styledflower,showingtwo
developedseeds.Allscalebars(cid:1)2mm.
were long-styled morph and 51(cid:1) (21/41)
short-styled one. In the long-styled morph, a
style was exserted from the corolla tube and
bifurcated, forming a stigma, while stamens
remain within a corolla tube and their
anthers, especially their lower half, were
concealed with a number of long, oblique-
facing hairs (Figs. 1B, 3A ). In the short-
1
styled morph, on the other hand, stamens
with long filaments were exserted from the
corolla tube and their anthers dehisced
introrsely, and a style was positioned below
the anthers and its stigma was wholly con-
cealed with a number of oblique-facing hairs
born on the corolla tube (Figs. 1A, 3B).
1
Fig. 2. Scatter diagram showing a relationship of Between the two morphs there was no sig-
stigma height and anther height in Psychotria nificant difference in corolla-tube length
boninensis. (Table 1). However, the two morphs differed
significantly from each other in corolla
length and anther length (Table 1).
a natural population revealed the presence of Dissected flower buds of the two morphs
two distinct floral morphs: long-styled were examined to show the relation of
morph with short stamens and short-styled stigma height, anther height and position of
morph with long stamens (Figs. 1, 2). At the long hairs attached to the corolla tube. We
studysite,49(cid:1)(20/41)oftheplantssampled focused on the oblique-facing hairs borne on
254 植物研究雑誌 第82巻 第5号 平成19年10月
Table1. Comparisonoflong-andshort-styledmorphsinseveralfloralandreproductivecharactersof Psychotria
boninensis
Long-styled Short-styled
Floraltrait Statistics
Mean±SD(N)* Mean±SD(N)*
Corollalength(mm) 4.4±0.4(20) 4.7±0.3(21) 0.001<p<0.01
Corolla-tubelength(mm) 2.2±0.3(9) 2.3±0.2(12) ns
Stigmaheight(mm) 3.7±0.4(20) 1.9±0.3(21) p<0.001
Antherheight(mm) 2.4±0.3(20) 4.2±0.5(21) p<0.001
Antherlength(mm) 1.0±0.1(20) 1.1±0.1(21) 0.001<p<0.01
Diameterofpollengrain(µm) 38.1±1.9(20) 50.5±2.8(21) p<0.001
Pollennumberperflower 4460±762(10) 2887±462(10) p<0.001
Stainabilityofpollengrain((cid:1)) 94.9±5.6(20) 93.3±7.8(21) ns
*Nrepresentsnumberofindividualplantsexamined.
**Statisticstests(Student’s t-test)werecarriedoutbetweenlong-andshort-styledmorphs.
the corolla tube. In young flower buds of the morphs (Student’s t-test, p <0.001). As
two morphs, stamen height and style height shown in Table 1, average number of pollen
were equal to each other and the hairs were grainsperflowerwas4460inthelong-styled
positioned below the stigma and stamens morph and 2887 in the short-styled morph,
(Fig. 3A , B ). In flower buds before respectively,sothepollennumberperflower
3 3
anthesis,theoblique-facinghairsofthelong- of the long-styled morph was more than 1.5
styled morph were positioned below the times relative to that of the short-styled
stamens and stigma (Fig. 3A), like those in morph.
2
the mature flowers, while the hairs of the
short-styled morph concealed the stigma Stainability of pollen grains and fruit pro-
entirely (Fig. 3B). duction
2
Each of the two morphs showed high
Dimorphism in pollen size and number of pollen stainabilities. Average values were
pollen grains per flower 94.9(cid:1)for the long-styled morph and 93.3(cid:1)
Pollen grains from the two morphs were for the short-styled morph, respectively
spherical and tri-colporate in aperture (Fig. (Table 1). Statistically, there was no signifi-
4). Polar diameter of pollen grains from the cant difference between the two morphs in
short-styled morphs was significantly longer pollen stainability (Student’s t-test, p >
than those from the long-styled morphs 0.05).
(Student’s t-test, p < 0.001; Fig. 5, Table 1). Meanwhile, flowers of the two morphs
Exine sculpture of pollen grains from the often produced fruits under natural popula-
both morphs showed complex reticulation. tions, and their fruits usually contained two
Between the two morphs, no major differ- seeds in each ovary (Fig. 1A’, B’), although
ence was found in exine sculpture (Fig. 4). the fruit and seed productions of the two
Number of pollen grains per flower was morphs were not examined quantitatively in
compared between the two morphs. the present study. It is certain that the pistils
Although the number of pollen grains per of the two morphs are functional, since they
flower varied considerably within a plant or produce fruits and seeds.
among plants, it significantly differed
between the long- and the short-styled
October2007 JournalofJapaneseBotanyVol.82No.5 255
Fig.3. SEMphotographsofflowersandflowerbudsinlong-andshort-styledmorphsofPsychotriaboninen-
sis.A.Long-styledflowerafteranthesis.A.Long-styledflowerbeforeanthesis.A.Youngflowerbudof
1 2 3
long-styled morph. B. Short-styled flower after anthesis, in which stigma was covered with a number of
1
oblique-facing long hairs. B. Short-styled flower before anthesis. B. Young flower bud of short-styled
2 3
morph,inwhichstigmawasexsertedfromtheupward-facinghairs.
256 植物研究雑誌 第82巻 第5号 平成19年10月
Fig. 4. SEM photographs of pollen grains in long- and short-styled morphs of Psychotria boninen-
sis. A.Pollen grain from a stamen in the short-styled morph. B. Pollen grain from a stamen in the
long-styledmorph.
flowers. In these respects the floral dimor-
phism found in P. boninensis is very similar
to that of the typically distylous (hetero-
stylous) species reported so far (Ganders
1979, Barrett 1992, Dulberger 1992,
Sugawara et al. 2002). Therefore, P.
boninensisendemictotheBoninIslandsmay
beregardedasdistylous,likeotherspeciesof
this genus (Ganders 1979, Hamilton 1989),
although there still remains uncertainty as to
whether the species has an incompatibility
system that prevents self and intramorph
matings. This is the first record on stylar
dimorphism from the plants endemic to the
Fig.5. Polardiameterofpollengrainsfromlong-and Bonin Islands.
short-styled morphs of Psychotria boninensis. In the oceanic Hawaiian Islands, it is well
Vertical lines indicate standard deviations. known that dioecy is frequent among en-
SamplesizeandstatisticsrefertoTable1.
demic species (Carlquist 1974, Baker and
Cox 1984, Sakai et al. 1995). As already
stated in the introduction, all of the
Discussion Psychotria species (11 species) within the
The present studies revealed that the flow- islandsarefunctionallyunisexual(dioecious)
ers of Psychotria boninensis were morpho- despite their distylous nature in floral mor-
logically distylous and reciprocally differed phology (Wagner et al. 1990, Sakai et al.
in stigma and anther height. Moreover, pol- 1995). In the species concerned here, P.
len grains from the short-styled morph were boninensis, the long- and short-styled flow-
larger than those from the long-styled ers have fertile pollen grains and produce
morph, and the short-styled flowers pro- fruits and seeds under natural conditions.
duced less pollen grain than the long-styled These results suggest that the reproductive
October2007 JournalofJapaneseBotanyVol.82No.5 257
nature of P. boninensis is functionally bisex- References
ual, in contrast with that of the Hawaiian Baker H. G. and Cox P. A. 1984. Further thoughts on
Psychotria species. dioecism and islands. Ann. Missouri Bot. Gard.
An interesting feature in the flowers of 71:244–253.
Barrett S. C. H. 1992. Heterostylous genetic polymor-
Psychotria boninensis is the oblique-facing
phism: Model systems for evolutionary analysis.
long hairs found on the corolla tube of the
In:BarrettS.C.H.(ed.),EvolutionandFunctionof
two morphs. Contrary to that of the long- Heterostyly.pp.1–29.Springer-Verlag,Berlin.
styled morphs, the stigmatic surface of the ,WilkenD.H.andColeW.W.2000.Heterostyly
short-styled morphs is wholly concealed by in the Lamiaceae: the case of Salvia brandegeei.
PlantSyst.Evol. 223:211–219.
a number of the long oblique-facing hairs
Carlquist S. 1974. Island Biology. Columbia Univer-
on the corolla tube (Fig. 3). Such hairs may
sityPress,NewYork.
be common in the genus but are rarely found
Dulberger R. 1992. Floral polymorphisms and their
in the other genera of the same family functional significance in the heterostylous syn-
(Hamilton 1989). In general, the hairs found drome. In: Barrett S. C. H. (ed.), Evolution and
on the corolla tube are regarded as excluding Function of Heterostyly. pp. 41–84. Springer-
Verlag,Berlin.
nectar or pollen robbers such as syrphids
Ganders F. R. 1979. The biology of heterostyly. New
and/or as preventing evaporation of nectar
ZealandJ.Bot. 17:607–635.
from the corolla (Naiki and Kato 1999). We Hamilton C. W. 1989. A revision of Mesoamerican
have no evidence for these suggestions in Psychotria subgenus Psychotria (Rubiaceae). Part
our study species. Meanwhile, if the corolla 1: Introduction and species 1–16. Ann. Missouri
Bot.Gard. 76:67–111.
tube has no hairs that conceal a stigmatic
Kato M. and Nagamasu H. 1995. Dioecy in the en-
surface, clogging by the self-pollen grains
demic genus Dendrocacalia (Compositae) on the
may occur on the stigma, especially of the
Bonin(Ogasawara)Islands.J.PlantRes.108:443–
short-styled morph, as noted in the flowers 450.
of Daphne kamtchatica var. jezoensis KawakuboN.1990.DioecismofthegenusCallicarpa
(Kikuzawa 1989). Therefore, it seems prob- (Verbenaceae) in the Bonin (Ogasawara) Islands.
Bot.Mag.Tokyo 103:57–66.
able that the long hairs found on the corolla
Kikuzawa K. 1989. Floral biology and evolution of
tube of P. boninensis prevent landing of the
gynodioecism in Daphne kamtchatica var. jezoen-
pollen grains from the same flowers in polli- sis.Oikos 56:196–202.
nation system. To clarify these speculations, Naiki A. and Kato M. 1999. Pollination system and
further studies especially on pollination sys- evolution of dioecy from distyly in Mussaenda
parviflora (Rubiaceae). Plant Species Biology 14:
tems are needed.
217–227.
In conclusion, the present results indicate
Nepokroeff M., Bremer B. and Sytsma K. J. 1999.
that the flowers of Psychotria boninensis en-
Reorganization of the genus Psychotria and tribe
demic to the Bonin Islands are morphologi- Psychotrieae (Rubiaceae) inferred from ITS and
callydistylous,consistingoflong-andshort- rbcLsequencedata.Syst.Bot. 24:5–27.
styled morphs and reciprocally differ in Ono M. and Kobayashi S. 1985. Flowering plants
endemic to the Bonin Islands. In: Ono, M. and
stigmaandantherheight.Itisalsoconfirmed
Okumura K. (eds.), Endemic Plant Species and
that both long- and short-styled flowers of P.
Vegetation of the Bonin Islands. pp. 1 -96. Aboc-
boninensis are functionally bisexual. sha, Kamakura (in Japanese with English sum-
mary).
We thank to Dr. H. Kato for his help in Riveros G. M., Barría O. R. and Humaña P. A. M.
1995. Self-compatibility in distylous Hedyotis
field survey. We are also grateful to the
salzmannii(Rubiaceae).Pl.Syst.Evol. 194:1–8.
Environmental Agency of the Japanese
Sakai A. K., Wagner W. L., Ferguson D. M. and
Government, for permission to collect sam-
Herbst D. R. 1995. Origins of dioecy in the
ples used in this study. Hawaiianflora.Ecology 76:2517–2529.
258 植物研究雑誌 第82巻 第5号 平成19年10月
Sohmer S. H. 1977. Psychotria L. (Rubiaceae) in the Revised.Aboc-sha,Kamakura(inJapanese).
HawaiianIslands.Lyonia 1:103–186. Wagner W. L., Herbst D. R. and Sohmer S. H. 1990.
Sugawara T., Tanaka N., Murata J. and Zaw K. M. Manual of the Flowering Plants of Hawaii 2.
2002. Dimorphism of pollen grains and stigmas in UniversityofHawaiiPress,Honolulu.
the Heterostylous subshrub, Reinwardtia indica YamazakiT.1989.Rubiaceae.In:SatakeY.,HaraH.,
(Linaceae) in Myanmar. Acta Phytotax. Geobot. WatariS.andTominariT.(eds.),WildFlowersof
53:173–180. Japan, Woody Plants II: 190–204. Heibonsha,
, Watanabe K., Kato H. and Yasuda K. 2004. Tokyo(inJapanese).
Dioecy in Wikstroemia pseudoretusa (Thymelaea- . 1993. Psychotria L. In: Iwatsuki K., Yamazaki
ceae) endemic to the Bonin (Ogasawara) Islands. T., Boufford D. E. and Ohba H. (eds.), Flora of
ActaPhytotax.Geobot. 55:55–61. JapanIIIa:225–227.Kodansha,Tokyo.
Toyoda T. 2003. Flora of Bonin Islands, Enlarged &
近藤よし美a, 西出真人b, 渡邊謙太b, 菅原 敬b：
小笠原諸島固有植物オオシラタマカズラ (アカネ
科) における花の二型性 すなわち長花柱型と短花柱型の花を有し, それら
小笠原諸島固有植物オオシラタマカズラ (ボチョ の花粉のサイズは短花柱型よりも長花柱型におい
ウジ属) の花は形態的には単型であるとみなされ て有意に小さく, 花当たりの花粉生産量も長花柱
てきた (Ono and Kobayashi 1985, Yamazaki 1989, 花において有意に多いという結果が得られた. こ
1993, Toyoda 2003). ところが野外調査を通じて, れらは他の二型花柱性植物群に一般に見られる特
この種の花は同属内に一般に知られる二型花柱性 徴ともよく一致する. 一方機能的には, いずれの
である可能性が出てきた. 小笠原諸島同様に海洋 花型でも花粉はコットンブルー染色液に90(cid:1)以上
島として知られるハワイ諸島では, ボチョウジ属 の染色性を示し, またそれぞれの花は野外で果実
植物が11種 (いずれも固有種) 分布するが, その や種子をつくっていた. これらの結果は, オオシ
すべてが二型花柱性的特徴を有し, 一方で機能的 ラタマカズラ二型花がハワイ諸島のように機能的
には単性化し雌雄異株へと進化していることが報 単性花にならず, 両性花であることを示している.
告されている (Sohmer 1977, Wagner et al. 1990, 二型花柱性は小笠原諸島固有植物では初めての確
Sakai et al. 1995). そこで小笠原諸島のオオシラ 認であるが, 同属のもう一種についても同様の調
タマカズラが本当に二型花柱性を示すかどうかを 査を現在進めている.
確認するとともに, その性的機能についても調べ (a東京都立大学理学部生物学科,
た. その結果, オオシラタマカズラは二型花柱性, b首都大学東京大学院理学研究科牧野標本館)